A singular PpaA/AerR-like protein in Rhodospirillum rubrum rules beyond the boundaries of photosynthesis in response to the intracellular redox state

ABSTRACT Photosynthesis (PS) in Purple Non-Sulphur Bacteria (PNSB) is strictly controlled to avoid energy consumption and to prevent oxidative stress when oxygen is present. PpsR, a transcriptional repressor codified in the Photosynthetic Gene Cluster (PGC), is one of the main players in the regulation of PS related genes. In some cases, PpsR do not sense the environmental cue by itself but delegates this task to another protein like PpaA/AerR anti-repressors, which can ultimately affect PpsR affinity to some promoter regions. In this work, the effects of locus Rru_A0625 product (HP1) on PS regulation of Rhodospirillum rubrum , were studied by mutation/complementation and transcriptomic strategies. Rru_A0625 is located next to ppsR gene, just like other PpaA/AerR members, and its deletion annuls pigment synthesis in dark micro/anaerobic growth conditions. HP1 shows similarity to PpaA/AerR anti-repressors family, although it does not possess their typical cobalamin binding domain. A transcriptomic analysis of Rru_A0625 deletion mutant showed that HP1 not only has effects on bacterioclorophyll and carotenoid biosynthesis, but also many other biological processes in the cell. The most notorious is the impact on the transcription of the nitrogenase complex components and some accessory proteins. Our results suggest that this new member of the PpaA/AerR family has evolved losing the canonical cobalamin binding domain, but not the redox sensing capability, conserving a not fully understood mechanism of PS regulation. IMPORTANCE Rhodospirillum rubrum vast metabolic versatility places it as a remarkable model bacterium and an excellent biotechnological chassis. The key component of PS studied in this work (HP1) stands out among the other members of PpaA/AerR anti-repressors family since it lacks the most conserved motif they all share: the cobalamin B-12 binding motif. Even with a minimized and barely recognizable aminoacidic sequence, HP1 stills controls PS as the other members of the family, allowing a fast response to changes in the redox state of the cell. This work also shows that HP1 absence affects genes form relevant biological processes other than PS, including nitrogen fixation and stress response. From a biotechnological perspective, HP1 could be manipulated in approaches where PS is not necessary, such hydrogen or polyhydroxyalkanoates production, to suppress unnecessary energy burden.